The branches a through d designate the base of the NFC a , C. Species without a family label each belong to a separate family: A. Of these, MergedOrthoGroups For branches leading to C. Of these, 1, MergedOrthoGroups The 1, MergedOrthoGroups included a subset of core MergedOrthoGroups 9 universally nodule-enhanced, 10 universally root-enhanced. The pattern of scenarios not rejected in the analysis of the core MergedOrthoGroups was similar to that of the overall results: Among the core MergedOrthoGroups that did not reject a change of selection pressure at branch a i.
In addition, among the core MergedOrthoGroups that did not reject changes in selection pressure at branches b , c , and d, most Both C. Our analysis supports the homology shared by common descent of RNS among the three plant species based on multiple lines of evidence. First, orthologs for most of the 19 RNS pathway genes required for the proper nodulation in M.
Transcripts with high sequence similarity were found, even for the few genes that did not have an ortholog predicted Figure 1 and Table 2. This is the first time, to our knowledge, that the entire pathway has been detected comprehensively in the context of a phylogenetically based orthology framework.
The presence and the expression of orthologs across these three species indicates that their existence predates the NFC, which is required for the RNS to share a common function and common origin across them. For example, the Pearson correlation coefficient between the gene expression patterns between two sets of 20 plants in one species, Arabidopsis thaliana, was 0.
By contrast, the comparisons made in our study are between pairs of different plant species that have been diverging for nearly million years Bell et al. TABLE 4. These results strongly support the homology of RNS in all three lineages, i. It is possible that other factors, such as similarity in the age of these tissues across the three transcriptomes, may have contributed to the similarity of the gene expression patterns. An increased spatiotemporal resolution for C. With the inclusion of C. Because the initiation and establishment of RNS consists of multiple developmental stages Pawlowski and Demchenko, ; Roux et al.
Thus, genes that are up-regulated relative to root in the whole nodule are expected either 1 to be so strongly nodule-enhanced in a given stage that they are detected as up-regulated even after averaging expression values over the whole nodule, or 2 to be nodule-enhanced throughout the process of nodulation.
The latter expression pattern has been well documented in the case of NIN Schauser et al. For the remaining genes, whose orthologs were not universally up-regulated in either nodules or roots some were up-regulated in two hosts and non-significant in the third , a higher resolution of space and time would be helpful for accurate comparisons across species.
Among the processes found to be universally enriched in either nodules or in roots among the core genes, we focused on the following four processes based on the potential relevance to RNS. Orthologs of NRT1. However, there are no functional conducting xylem elements in root meristems of higher plants, which would be the tissue equivalent of Zone I of the root nodule. Moreover, nitrate is known to suppress nodulation in Ceanothus Thomas and Berry, and in L.
Taken together, these lines of evidence suggest that the function of NRT1. While the understanding of NRT1. The genetic dissection of RNS has revealed that the pathway for its establishment shares many of its genes with the more ancient pathway to form AM symbiosis Oldroyd, It is thus of substantial importance that D27 and MAX4 , genes coding for the enzymes of the first and the third steps of strigolactone biosynthesis Ruyter-Spira et al. Strigolactone has a number of functions in plants Besserer et al.
Strigolactone is also a signaling molecule that initiates AM symbiosis by stimulating the branching and growth of hyphae of the AM fungi Besserer et al.
Within the mature AM symbiotic tissue, however, strigolactone is down-regulated Kapulnik and Koltai, A similar pattern may be inferred for RNS. Strigolactone has been shown to play a role in promoting nodulation in Pisum sativum , in that a strigolactone mutant formed fewer nodules than wild-type Foo and Davies, , although, strigolactone is not required for nodulation, since nodulation does occur in the mutant.
The influence of strigolactone on nodulation in P. Thus, the down-regulation of strigolactone biosynthesis in the nodule tissue of three phylogenetically distinct hosts that was observed in this study could be a function derived from AM symbiosis, to inhibit a portion of the root system from forming further infection sites, or to limit a stage of root development from further growth, allowing for nodule development or maintenance.
The enrichment of the GO term related to secondary shoot formation in the root transcriptome is likely related to the pattern of strigolactone gene expression observed, since MAX4 plays a role in regulating branching in the shoot Sorefan et al. Cytokinin in legume RNS is a major signal to the cortical cells to initiate nodule organogenesis by induction of NIN through the activation of a cytokinin receptor LHK1 Tirichine et al.
Since the up-regulation of NIN has been found in the nodules of A. We found a universal up-regulation of CYPA , a gene coding for the biosynthesis of trans-zeatin. IPT was also up-regulated in the nodules in C. Although IPT was down-regulated overall in M.
The cellular response to NO was universally down-regulated in the nodules of the three host plants in this study. Two sets of orthologs responsible for this pattern were detected, but only one had an assigned name: AHK5 , a histidine kinase originally identified in A. Since the nodules used in this study were all in relatively early stages of development, NO production in the nodules would not be expected to be high. Moreover, NO binds to and reduces activity of glutamine synthetase Melo et al.
Thus, the down-regulation of AHK5 would be important to maintain low concentrations of NO in the nodules. Alternatively, in Arabidopsis , AHK5 is known to confer resistance to pathogens such as Pseudomonas syringae and Botrytis cinerea Pham et al. Moreover, AHK5 was most highly expressed in the roots of A. An inverse relationship exists between the host plant immune response and symbiotic processes established in the root nodules Toth and Stacey, Down-regulation of AHK5 could be part of the mechanism that enables the harboring of bacterial cells within the plant cells.
Of the 3, MergedOrthoGroups, Of these 1, MergedOrthoGroups, Among these, only 0. The 58 core genes MergedOrthoGroups , which should be strong candidates for playing key roles in the evolutionary origin of RNS, showed the same general pattern: Among these, We did not determine how many, if any, of the MergedOrthoGroups i.
However, the results of analyzing nearly 4, genes clearly disfavor the single-origin hypothesis. Even the MergedOrthoGroups that rejected the TWOSTEP scenario are not in conflict with the two-step hypothesis, because the two-step hypothesis does not require the same gene to be responsible for both the gain-of-predisposition and the subsequent gain-of-function.
The evolution of RNS represents a major event in the biology of plant-microbe interactions Doyle, , and different explanations of the evolutionary origins have been proposed. We have demonstrated the genetic homology of RNS in the three lineages based on the presence of RNS pathway orthologs and the high similarity of gene expression patterns across the three species, thus demonstrating that RNS shares a common evolutionary event at the base of the NFC.
At the same time, we show that most genes regardless of whether the gene is involved in the process of RNS or not that experience change in selection pressure at the base of the NFC also experienced subsequent changes in selection pressure at the base of each RNS host lineage. Taken together, our results are most consistent with the two-step hypothesis of the origin of RNS. The work of Werner et al.
Our findings provide additional support for the two-step hypothesis. On the other hand, two recent papers suggest a more ancient origin of functional RNS within the NFC followed by multiple losses Griesmann et al. Within a single genus, Dryas octopetala Rosaceae apparently does not form root nodules, whereas other Dryas species retain this trait Becking, Since the known functions of these genes are specific to RNS, multiple losses are difficult to explain under two-step hypothesis where these genes would be maintained for millions of years after the gain-of-predisposition event until the gain-of-function event.
What is the genetic nature of the predisposition assumed in the two-step hypothesis? Otherwise, the propensity for a gain-of-function could not have been conserved for tens of millions of years in multiple lineages Doyle, ; Werner et al. Likewise, a single-origin hypothesis needs an explanation for its apparently unparsimonious distribution of RNS hosts within the NFC. The high cost of RNS might be an explanation Griesmann et al.
In either case, the key to answer this question depends on an understanding of the genetic underpinnings that led to RNS, which still remains incomplete. Ceanothus thyrsiflorus var. Shortly after arrival, original media was removed and the plants were transplanted into Stuewe D40H pots 6.
The roots were inoculated at the time of transplant. No preexisting root nodules were observed in any plants. The soil inoculum was directly applied to the exposed root ball.
Datisca glomerata seeds were collected from wild D. Seedlings were irrigated daily with deionized water. The roots were then cut back and repotted with fresh media. Three days after the roots had been collected, seedlings were inoculated. Crushed nodules were collected from a different set of D. These previous seedlings had been inoculated with crushed nodules that originated from the same inoculum source as the C.
Roots tips and nodules of both C. The C. For roots, root tips approximately 2. To remove media particles, roots or nodules were rinsed in deionized water immediately before flash freezing in liquid nitrogen.
The sampling process was kept under 5 min per plant. The libraries were pooled in equimolar ratios for sequencing. For C. For D.
Raw sequence reads were trimmed based on read quality and adapter contamination using Scythe v0. Insert sizes were verified using Bowtie2 v2. Because neither the C. The controls were selected based on the reference genes tested in Medicago sativa Castonguay et al. Default settings were used except the size of the product was limited to 90— bps. PCR primers were chosen to amplify a segment near the middle of the transcript. Roots and root nodules were sampled from three different individuals of C.
Here, the nodules of C. Once the threshold cycle C T was determined for each reaction, the average C T for each gene was calculated for each tissue for each species. Published root and nodule 15 days after inoculation transcriptome data were obtained from a previous study Roux et al.
The genome sequence of M. For genes that were not expressed in either of the tissues, the expression levels, the log2-fold changes, and the associated p -values were considered 0, 0, and 1, respectively. Henceforth, M. The M. BUSCO v2. Analyses of differential gene expression between the two tissues nodule and root for C.
Expected reads for each gene were estimated by using RSEM v1. For M. The p -value threshold for C. GO enrichment analysis was conducted using R v3. After calculating the raw p -values, to account for multiple testing, the significance of each GO term was tested through Benjamini—Hochberg procedure. To enable the comparison of orthologous sets of genes across and beyond the NFC, a nucleotide sequence database was constructed with 12 genomes total CDSs from species within the NFC and close outgroups in combination with the C.
These sequences were collected from three different databases: Phytozome v11 Goodstein et al. These sequences were removed from the analyses. In order to capture orthologs beyond the in-paralogs Sonnhammer and Koonin, expected from the genome duplications in Fabaceae Cannon et al.
For genes with multiple isoforms or alleles, orthologs were predicted independently for each member, and the union of the predictions of all isoforms was considered the set of predicted orthologs for the gene. The predicted orthologs were then merged into 27, non-overlapping MergedOrthoGroups using a custom Perl script Supplementary Table S5.
In addition, orthologs of 19 genes from M. Reference sequences for these 19 RNS pathway genes were collected from GenBank, and verified in the database assembled in this study. OrthoReD with the same parameter settings as other sequences were used to predict orthology for L. For each of the 19 RNS pathway genes, a set of genes was collected comprising every C. From the 27, MergedOrthoGroups, we first parsed out whole MergedOrthoGroups, each of which: 1 contained at least one member from each of C.
We also parsed subsets within the remaining MergedOrthoGroups that met the aforementioned two criteria only with respect to the three species C. Then the gene expression pattern was scored as root-enhanced, nodule-enhanced, or not significantly different between the two tissues based on the differential gene expression analysis for each species for each MergedOrthoGroup.
For MergedOrthoGroups where a single species was represented by more than one paralog, the gene expression pattern for this species was considered root- or nodule-enhanced if there was at least one significantly differentially expressed paralog, unless one or more of them were enhanced in one tissue and other paralog s were enhanced in the other tissue, in which case the MergedOrthoGroup was considered to be both root- and nodule-enhanced for that species.
Among the representative MergedOrthoGroups, those that were either nodule-enhanced or root-enhanced in all three species were collected and designated as the core MergedOrthoGroups. Next, we tested how strongly the differences in gene expression between roots and nodules in each species are correlated with those of other species using the approach previously applied for measuring the similarities between biological replicates Kempema et al.
For each pair of species, the gene expression level fold changes between the two tissues were plotted for all MergedOrthoGroups. The Pearson correlation coefficient was then calculated separately for all MergedOrthoGroups, for MergedOrthoGroups that were nodule-enhanced in both species, and for those that were root-enhanced in both species using cor.
For MergedOrthoGroups where at least one of the species was represented by more than one paralog, the most similar pair of fold changes was used as the representative. Finally, the degree and significance of overall similarity in gene expression between each pair of species was assessed using dissonance scores summarized in Supplementary Image S2.
For each pair of species for each MergedOrthoGroup, the degree of dissonance between the species was calculated as the average pairwise difference in fold change between all transcripts for the two species belonging to that group for some groups, one or more species was represented by more than one transcript. Next, the overall dissonance score between species A and B was calculated as the total sum of the dissonance scores of all representative MergedOrthoGroups.
Finally, in order to determine the statistical significance of this measure, a permutation test random resampling of fold change values with no replacement was conducted to calculate the overall dissonance score for 10, replicates, and the p -value was calculated as the fraction of permutations that yielded an overall dissonance score equal to or smaller than the observed data.
The normal distributions of the total dissonance scores among the permutations were verified using R v3. The aforementioned 3, MergedOrthoGroups, i. The three competing hypotheses single-origin, multiple-origin, and two-step hypothesis differ in the expected timing s of gaining predisposition or function of RNS, the events that would have caused changes in selection pressures on the genes involved.
To serve as the basis for comparisons between these scenarios, a multiple sequence alignment MSA and a most-likely gene phylogeny were generated for each MergedOrthoGroup. Two phylogenetic trees were constructed using RAxML v8. The topology of one tree was constrained to the family level according to the established phylogeny APG, see Figure 4 as a reference , while the topology of the second tree was not constrained.
For each tree, four parallel searches were carried out to prevent lodging on to local optima. In some MergedOrthoGroups for which the unconstrained topology was used, some scenarios were not tested because the clade required for the scenario was missing from the tree. Based on the results generated by the methods described above, the three competing hypotheses single-origin, multiple-origin, and two-step were tested against each other. The multiple-origin hypothesis differs from the other two hypotheses in that it assumes completely independent gains of RNS in different lineages.
A significant result would indicate the presence of a common evolutionary background among the three species compared which are phylogenetically distantly related species distributed throughout the NFC , supporting single-origin or two-step hypothesis, and rejecting the multiple-origin hypothesis. Among MergedOrthoGroups that rejected the NULL scenario, MergedOrthoGroups that fail to reject only the MULTI scenario would be consistent with both the multiple-origin hypothesis and the two-step hypothesis, because the two-step hypothesis does not require the same gene to be the cause of both the gain-of-predisposition and the gain-of-function.
However, such genes would be in conflict with the single-origin hypothesis because additional changes for each RNS host lineage are not assumed in this hypothesis. Likewise, genes that fail to reject only the SINGLE scenario would be consistent with either the single-origin hypothesis or the two-step hypothesis, but would be in conflict with the multiple-origin hypothesis.
Finally, genes that fail to reject only the TWOSTEP scenario would be in conflict with both the multiple-origin and single-origin hypotheses, and would only be consistent with the two-step hypothesis. KB conducted the experiments, analyzed the data, and substantially wrote the manuscript. JC, DP, and AB provided suggestions on the experimental design, interpretations for comparative transcriptomics, phylogenetics, and the biology of RNS, and contributed to editing the manuscript.
AB provided an initial project framework. UC Davis Bioinformatics Core pilot grant KB supported access to the high-performance computing cluster needed to conduct this research. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank Isaac Gifford for insightful discussions.
We also thank Ernest K. Lee, Dr. Monica Britton, and Dr. Lutz Froenicke for advice on high-throughput sequencing data, Dr. Blythe P Durbin-Johnson on differential gene expression analysis, Dr. Neil Willits for advice on statistical analyses, and Dr. Brian Moore for advice on phylogenetic analyses. Alexa, A. Topgo: Enrichment Analysis for Gene Ontology.
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The nodule structure is largely determined by the plant [ 80 ]. The major regulators of nodule development are phytohormones. Some of them play distinct or even opposite roles in the organogenesis of determinate and indeterminate nodules [ 81 ].
Plant hormones are also produced by rhizobia and these may too affect nodulation process [ 82 ]. The rhizobia studied here, induced cylindrical nodules on the A. Anatomically, the liquorice milkvetch nodules were differentiated into persistent apical meristem, bacteroid tissue consisting of infected and uninfected cells, as well as multi-layered nodule cortex, with a vascular system Fig 5A.
Within the bacteroid tissue, a developmental zonation was discernible Fig 5A. Proximal to nodule meristem, cells were penetrated by infection threads Fig 5B and infected endocytotically by rhizobia, which was a symptom of the onset of bacteroid tissue differentiation. In the infected cells, differentiation involved considerable cell growth, symbiosome multiplication, proliferation of membranous organelles and the decrease of vacuolation.
Gradually, the amyloplasts were formed and together with closely-associated mitochondria they were translocated into the vicinity of intercellular spaces. The general anatomy and ultrastructure of A. Thin arrows—mitotic cells; thick arrows—the most distant infection threads visible in section; IT—infection threads, arrowheads—delimitation of a meristematic apex of vascular bundle; open arrowheads—lateral delimitation of the differentiating bacteroid-containing tissue note that in this region the inner cortex is only two cells wide.
Open rosette—plastid note its close association with mitochondria ; rosette—starch grains; slim arrows—dividing bacteroids; arrowhead—dictyosome; open arrowheads—rough endoplasmic reticulum cisterns; M—mitochondria; niC—non-infected cell; IS—intercellular space; CW—cell wall; B—bacteroids.
Slim arrows—invaginations of bacteroid's cytoplasmic membrane; arrowhead—fine-granular inclusion; open arrowheads—poly-beta-hydroxybutyrate granules; white arrowheads—peribacteroid membrane.
The symbiosome ultrastructure in the senescent cell of the bacteroid-containing tissue of A. Slim arrows—invaginations of bacteroid's cytoplasmic membrane; arrowhead—fine-granular inclusion; open arrowhead—poly-beta-hydroxybutyrate granule; white arrowheads—peribacteroid membrane; double arrowheads—bacteroid's cell wall; PS—peribacteroid space.
The saprotrophic zone of the bacteroid-containing tissue of A. Black asterisks—degraded infected cells; thin arrows—compressed remnants of degraded bacteroids; white asterisks—matrix in degraded cells populated by of saprotrophic rhizobia; thick arrows—infection threads; arrowheads—colonies of saprotrophic rhizobia.
In the symbiosomes, peribacteroid space was narrow Fig 5D. Bacteroids were rounded or slightly elongated in sections, with both outer and cytoplasmic membranes the latter forming occasional invaginations clearly discernible. Gradually, the senescence zone was formed due to the degenerative changes in the ultrastructure of symbiosomes Fig 5E.
The peribacteroid space widened locally and bacteroids' cytoplasm became heterogeneous Fig 5E. Invaginations of the cytoplasmic membrane gradually increased and took the shape of intricately twisted tubules. Concurrently, the degenerative changes occurred in the host organelles and tonoplast became fragmented not shown. Infection threads with intact rhizobial cells were visible in the senescent zone. At the proximal end of the bacteroid tissue, closest to the point of attachment to the "parent" root, a large saprotrophic zone was formed Fig 5A.
They were embedded in a fibrillar matrix, which had a characteristic pinwheel pattern Fig 5F resulting from the orderly arrangement of fibrils. The bacteroid tissue of nodule was surrounded by lateral tissues: a the multilayered inner cortex with vascular bundles, b the monolayered cortical endodermis, built of tightly-arranged cells and c an outer cortex of loose parenchyma Fig 5A.
Generally, the anatomy of A. In summary, the six A. The most plausible explanation for incongruence between phylogenies based on 16S rRNA and symbiosis genes, seems to be the lateral transfer of symbiotic information, from a common ancestor to the bacteria studied. Rhizobia specific to A. Nodules induced on liquorice milkvetch roots are typically indeterminate, in terms of their histological structure. Conceived and designed the experiments: SG WM.
Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract The phylogeny of symbiotic genes of Astragalus glycyphyllos L. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Data Availability: All relevant data are within the paper.
Introduction Rhizobia are soil bacteria, capable of forming nitrogen-fixing symbiosis with fabacean plants, which is beneficial for agriculture and other environmental systems [ 1 , 2 ].
Phylogenetic analysis The symbiotic genes sequences of A. Plant tests All 28 A. Statistical analysis of plant-test data Date from plant tests, concerning symbiotic interaction of A. Light and electron microscopy For microscopy studies, inoculated A. Results and Discussion Effective symbiosis between rhizobia and fabaceans, initiated by nitrogen starvation of the host plant, requires several bacterial symbiotic genes, including nitrogen-fixation nif ones, determining the reduction of N 2 into ammonium and nodulation nod genes that encode Nod factors triggering nodule formation [ 7 , 8 , 49 — 51 ].
The nodA gene phylogeny The nodulation gene nodA determines the type of N-acyl substitution on the nonreducing end of the Nod factor core and thus plays a significant role in determining the symbiotic specificity of nodule bacteria [ 8 , 38 , 53 ].
Download: PPT. Fig 1. Maximum-likelihood phylogenetic tree based on partial nodA gene sequences of A. The nodC gene phylogeny The nodC gene encoding N-acetylglucosaminyltransferase, responsible for the first step in Nod factor assembly, is related to the host range of the nodule bacteria [ 7 , 12 ]. Fig 2. Maximum-likelihood phylogenetic tree based on partial nodC gene sequences of A. The nodH gene phylogeny The nodH gene, which encodes sulfotransferase involved in the transfer of a sulfate group to the reducing end of the Nod factors [ 7 , 14 , 67 — 69 ], was identified in the A.
Fig 3. Maximum-likelihood phylogenetic tree based on partial nodH gene sequences of A. The nifH gene phylogeny In our present study, on the phylogeny of symbiotic genes of A.
Fig 4. Maximum-likelihood phylogenetic tree based on partial nifH gene sequences of A. Host range and symbiotic efficiency Rhizobia forming N 2 fixing interactions with fabaceans exhibit various degree of symbiotic specificity, from very narrow as in the case of bacteria associated with plants of tribes; Trifolieae, Cicereae or Viceae [ 7 ] to broad host range promiscuous as for example strains isolated from nodules of L.
Table 1. Nitrogen-fixing efficiency of A. The microscopic structure of A. Fig 5. The structure of A. References 1. Legume growth-promoting rhizobia: An overview on the Mesorhizobium genus. Microbiol Res. Zahran HH. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev. Bacterial associations with legumes.
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